ISSN (Print) 0023-4001 ISSN (Online) 1738-0006

Korean J Parasitol Vol. 57, No. 5: 521-524, October 2019 ▣ BRIEF COMMUNICATION https://doi.org/10.3347/kjp.2019.57.5.521

Soboliphyme baturini (Nematoda: Soboliphymatidae) Recovered from Stomach of Asian , leucurus, in Geochang-gun, Gyeongsangnam-do,

Woon-Mok Sohn*, Byoung-Kuk Na Department of Parasitology and Tropical Medicine, and Institute of Health Sciences, Gyeongsang National University College of Medicine, Jinju 52727, Korea

Abstract: We are going to describe the female soboliphymid nematodes, which were recovered from the stomach of a Asian badger, Meles leucurus (Mammalia: ), in Geochang-gun, Gyeongsangnam-do, Korea. In February 1998, we found 2 peculiar nematodes with a cup-like organ in the anterior end from the stomach of badger. Recovered worms were fixed with 10% formalin, cleared in glycerin-alcohol solution and observed under a light microscope with a microm- eter. They were 34.46 (33.43-35.50) mm long by 2.13 mm at maximum width. Cephalic sucker cup-like, 3.34 (3.13-3.55) mm wide, 2.40 (2.25-2.55) mm long, with the oral aperture and meridionally striated on the buccal capsule. Oral aperture 2.38 mm in diameter. Circumoral membrane 0.41 (0.38-0.45) mm wide. Esophagus muscular, 4.81 (4.50-5.00) mm long by 0.80 (0.78-0.83) mm at maximum width. Vulva situated at 3.13 mm ventro-anterior level from the esophago-intestinal junction. Vagina anteriad, 3.38 mm long, making a canal from the uterus to the vulva opening. Uterus single, large. Tail 0.35 (0.33-0.38) mm long. Intrauterine eggs long elliptical, 0.058-0.065 (0.062) mm long and 0.030-0.033 (0.031) mm wide. Based on the some morphological characters and host-specificity, our specimens are nearly identical with S. ba- turini. Therefore, the present report describes S. baturini for the first time in Korea.

Key words: Soboliphyme baturini, Badger, Meles leucurus, Republic of Korea

Nematode members in the genus Soboliphyme (Nematoda: So- In February 1998, we obtained a whole set of visceral organs boliphymatidae) are the gastro-intestinal parasites of carnivores and some muscles of a badger from a wholesale house of ani- and insectivores. About 9 species, i.e., Soboliphyme abei, S. ataa- mals located in Geochang-gun, Gyeongsangnam-do, the Re- hai, S. baturini, S. caucasica, S. huridiniformis, S. jamesoni, S. occi- public of Korea (Korea) to examine the infection of Trichinella dentalis, S. soricis, and S. urotrichi, have been reported in the liter- larvae. We also examined helminthic infections from the bad- atures [1-7]. It has been known that soboliphymid nematodes ger and recovered 2 peculiar nematodes with a cup-like organ have 2 hosts in their life cycle. Larvae develop in oligochaetes, in the anterior end from the stomach. Recovered worms were earthworm, and adults dwell in the gastro-intestinal tract of in- fixed with 10% formalin, cleared in glycerin-alcohol solution sectivorous and carnivorous by the eating of interme- and observed under a light microscope with a micrometer. diate and/or paratenic hosts with larvae [2,3]. However, there are They were female worms with a cup-like structure in the an- no reports on the soboliphymid nematodes in Korean fauna. We terior and a pointed tail in the posterior ends. Their morpho- describe with 2 female soboliphymids recovered from the stom- logical characters were as follow (Fig. 1). Body 34.46 (33.43- ach of a Asian badger, Meles leucurus (Mammalia: Mustelidae), in 35.50) mm long and 2.13 mm at maximum width. Cephalic Geochang-gun, Gyeongsangnam-do, Korea. sucker cup-like, 3.34 (3.13-3.55) mm wide, 2.40 (2.25-2.55) mm long, with the oral aperture and meridionally striated on

Received 3 August 2019, revised 24 September 2019, accepted 25 September 2019. the buccal capsule. Oral aperture (opening) 2.375 mm in di- • Corresponding author ([email protected]) * ameter. Circumoral membrane 0.413 (0.38-0.45) mm wide. © 2019, Korean Society for Parasitology and Tropical Medicine Esophagus muscular, 4.81 (4.50-5.00) mm long and 0.80 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) (0.78-0.83) mm at maximum width. Vulva situated at 3.125 which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. mm ventro-anterior level from the esophago-intestinal junc-

521 522 Korean J Parasitol Vol. 57, No. 5: 521-524, October 2019

A B

C D

Fig. 1. (A) Two female worms of Soboliphyme baturini recovered in the stomach of badger, Meles leucurus, from Geochang-gun, Gyeongsangnam-do, Korea. (B) Magnified view of cephalic sucker with the oral aperture (OA) and meridionally striated on the buccal capsule. (C) Anterior portion with a characteristic cephalic sucker (CS), muscular esophagus (E), intestine (I), uterus (U), long vagina (V) and vulva opening (arrow). (D) Posterior portion with the uterus (U), intestine (I) and anus (arrow). Scale bar= 1 mm. Sohn et al.: Soboliphyme baturini from a badger in Korea 523

Table 1. Comparative dimensionsa of Soboliphyme spp. with those of previous studies

Present study S. baturini S. ataahai S. occidentalis Organs (Sohn et al., 2019) (Swartz, 1968) (Ganzorig et al., 2003) (Ribas et al., 2004) Body (BL) 33.43-35.50 (34.46) 17.5-24.1 23.6-35.8 (33.7) 21.89-24.62 (22.41) Body (BW) (2.13) 1.33-1.63 1.12-1.70 (1.40) 0.78-0.97 (0.95) Ratio of BW:BL 01:16.2 01:14.0 01:24.1 01:23.8 Cephalic capsule (L) 3.13-3.55 (3.34) 2.01-2.45 1.51-1.97 (1.66) 1.38-1.60 (1.51) Cephalic capsule (W) 2.25-2.55 (2.40) in diameter 1.48-1.70 (1.55) 1.27-1.38 (1.30) Esophagus (L) 4.50-5.00 (4.81) 3.04-4.02 3.30-4.58 (3.79) 4.32-4.38 (4.35) Locationb of vulva Anterior level Anterior level E-I junction level Posterior level Vagina (L) 3.38 - 2.36-2.92 (2.71) 0.73-0.95 (0.84) Tail (L) 0.33-0.38 (0.35) 0.14-0.32 0.47-0.64 (0.62) 0.30-0.43 (0.42) Eggs (L) 0.058-0.065 (0.062) 0.054-0.063 0.080-0.115 0.079-0.082 Eggs (W) 0.030-0.033 (0.031) 0.032-0.036 0.042-0.069 0.038-0.041 Host Asian badger Laxmann’s shrew Iberian mole Meles leucurus Neovison vison Sorex caecutiens Talpa occidentalis aOnly female worms: (L) length; (W): width; unit is mm. bLocation from esophago-intestinal (E-I) junction. tion. Vagina anteriad, 3.38 mm long, making a canal from the appear to be restricted to Asia, and only one species, S. jameso- uterus to the vulva opening. Uterus single, large. Tail 0.35 (0.33- ni, occurs in North America [3-5,11-14]. Only one species that 0.38) mm long. Intrauterine eggs long elliptical, 0.058-0.065 parasitizes in carnivores, S. baturini, is broadly distributed in (0.062) mm long and 0.030-0.033 (0.031) mm wide (Table 1). Eurasia and North America [3,15]. Among 9 soboliphymid nematodes reported in the litera- Six of the 9 soboliphymid nematodes previously reported, tures, 8 species, i.e., S. abei, S. ataahai, S. caucasica, S. huridini- i.e., S. ataahai, S. baturini, S. huridiniformis, S. occidentalis, S. sor- formis, S. jamesoni, S. occidentalis, S. soricis and S. urotrichi, are icis and S. urotrichi, have the notched cephalic sucker. Among detected in insectivores, shrews and moles. Only 1 species, S. these, only 2 species, S. baturini and S. huridiniformis, have the baturini, has been found in carnivorous mammals in adult vulva opening at the ventro-anterior from the esophago-intes- stage like in this study [1-7]. Over 32 species of mammals have tinal junction like in our specimens (Table 1). However, S. been listed as the hosts of this nematode species [8]. Adult huridiniformis is found only in the insectivores, moles. The 2 worms of S. baturini are most commonly detected in sable and specimens in this study are considerably larger than those of (Martes spp.), and less frequently found in ermine and previous descriptions for S. baturini [16,17], but similar with (Mustela spp.), (Gulo gulo), and mink (Neovi- those of S. sahalinense Shimakura and Odajima, 1934 [18], son vison) [8]. Larval and/or juvenile worms are found in shrew which has been considered to be a synonym of S. baturini [2,3]. (Sorex spp.), canids and felids, which acted as the paratenic Some limited points, i.e., lack of male worms and insufficient and incidental hosts in the life cycle. In the aspect of host- number of female samples, exist in this study, but our speci- specificity, our specimen is closely related with S. baturini. mens are closely identical with some morphologies of S. ba- Moreover, the , Meles meles, has been listed as turini. the definitive host of S. baturini [8-10]. Based on the some morphological characteristics and host- Soboliphymids residing in insectivores are known to be specificity, the soboliphymid nematodes recovered from the host-specific and restrictive in distribution. Cross infections stomach of badger were identified as S. baturini in this study. between soboliphymids of shrews and moles do not occur. Accodingly, we report for the first time that the Asian badger, Four Soboliphyme spp., S. abei, S. ataahai, S. jamesoni and S. sor- M. leucurus, serves as the definitive host for S. baturini, and this icis, have been detected from shrews and 4 species, S. caucasica, species of nematode is distributed in Korean peninsula. Fur- S. hirudiniformis, S. occidentalis and S. urotrichi, have been ther studies on the soboliphymid nematodes should be per- found from moles. On the other hand, 4 species, i.e., S. cauca- formed in insectivores as well as in carnivores to expand the sica, S. hirudiniformis, S. occidentalis and S. soricis, are distribut- nematode fauna in Korea. ed in Europe only, 3 species, S. abei, S. ataahai, and S. urotrichi, 524 Korean J Parasitol Vol. 57, No. 5: 521-524, October 2019

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